Head-mounted sensors reveal visual attention of free-flying homing pigeons

ABSTRACT Gaze behavior offers valuable insights into attention and cognition. However, technological limitations have prevented the examination of animals' gaze behavior in natural, information-rich contexts; for example, during navigation through complex environments. Therefore, we developed a lightweight custom-made logger equipped with an inertial measurement unit (IMU) and GPS to simultaneously track the head movements and flight trajectories of free-flying homing pigeons. Pigeons have a limited range of eye movement, and their eye moves in coordination with their head in a saccadic manner (similar to primate eye saccades). This allows head movement to act as a proxy for visual scanning behavior. Our IMU sensor recorded the 3D movement of the birds' heads in high resolution, allowing us to reliably detect distinct saccade signals. The birds moved their head far more than necessary for maneuvering flight, suggesting that they actively scanned the environment. This movement was predominantly horizontal (yaw) and sideways (roll), allowing them to scan the environment with their lateral visual field. They decreased their head movement when they flew solo over prominent landmarks (major roads and a railway line) and also when they flew in pairs (especially when flying side by side, with the partner maintained in their lateral visual field). Thus, a decrease in head movement indicates a change in birds' focus of attention. We conclude that pigeons use their head gaze in a task-related manner and that tracking flying birds' head movement is a promising method for examining their visual attention during natural tasks. Highlighted Article: A lightweight custom-made logger equipped with an inertial measurement unit (IMU) and GPS revealed head-gaze movement during homing flights in pigeons.

[1]  A. Kacelnik,et al.  Asymmetric visual input and route recapitulation in homing pigeons , 2015, Proceedings of the Royal Society B: Biological Sciences.

[2]  Andrew T. Duchowski,et al.  Eye Tracking Methodology: Theory and Practice , 2003, Springer London.

[3]  S. J. Phillips,et al.  Head orientation in pigeons: postural, locomotor and visual determinants. , 1989, Brain, behavior and evolution.

[4]  T. A. Hurly,et al.  Wild hummingbirds require a consistent view of landmarks to pinpoint a goal location , 2018, Animal Behaviour.

[5]  Esteban Fernández-Juricic,et al.  Sensory basis of vigilance behavior in birds: Synthesis and future prospects , 2012, Behavioural Processes.

[6]  Alexei L. Vyssotski,et al.  EEG Responses to Visual Landmarks in Flying Pigeons , 2009, Current Biology.

[7]  Á. Miklósi,et al.  Dogs' Gaze Following Is Tuned to Human Communicative Signals , 2012, Current Biology.

[8]  T. Vicsek,et al.  Hierarchical group dynamics in pigeon flocks , 2010, Nature.

[9]  J. Call,et al.  Eye tracking uncovered great apes' ability to anticipate that other individuals will act according to false beliefs , 2017, Communicative & integrative biology.

[10]  M. F. Land,et al.  The roles of head movements in the search and capture strategy of a tern (Aves, Laridae) , 1999, Journal of Comparative Physiology A.

[11]  David Lentink,et al.  How Lovebirds Maneuver Rapidly Using Super-Fast Head Saccades and Image Feature Stabilization , 2015, PloS one.

[12]  T. Vicsek,et al.  Robustness of flight leadership relations in pigeons , 2013, Animal Behaviour.

[13]  Mandyam V. Srinivasan,et al.  Optic Flow Cues Guide Flight in Birds , 2011, Current Biology.

[14]  D. Biro,et al.  Cumulative culture can emerge from collective intelligence in animal groups , 2017, Nature Communications.

[15]  Dora Biro,et al.  Homing pigeons (Columba livia) modulate wingbeat characteristics as a function of route familiarity , 2017, Journal of Experimental Biology.

[16]  M. Nagy,et al.  Misinformed leaders lose influence over pigeon flocks , 2016, Biology Letters.

[17]  A. Wohlschläger,et al.  Head and eye movements in unrestrained pigeons (Columba livia) , 1993 .

[18]  D. Sumpter,et al.  From Compromise to Leadership in Pigeon Homing , 2006, Current Biology.

[19]  Stephen V. Shepherd,et al.  Monkeys at the Movies: What Evolutionary Cinematics Tells Us about Film , 2011 .

[20]  David N. Lee,et al.  Where we look when we steer , 1994, Nature.

[21]  A. Fuchs Saccadic and smooth pursuit eye movements in the monkey , 1967, The Journal of physiology.

[22]  S. Kane,et al.  Falcons pursue prey using visual motion cues: new perspectives from animal-borne cameras , 2014, Journal of Experimental Biology.

[23]  Giorgio Vallortigara,et al.  Olfactory lateralization in homing pigeons: a GPS study on birds released with unilateral olfactory inputs , 2011, Journal of Experimental Biology.

[24]  Stephen Roberts,et al.  An edge-detection approach to investigating pigeon navigation. , 2006, Journal of theoretical biology.

[25]  David J. T. Sumpter,et al.  Interaction rules underlying group decisions in homing pigeons , 2013, Journal of The Royal Society Interface.

[26]  Dora Biro,et al.  Route following and the pigeon's familiar area map , 2014, Journal of Experimental Biology.

[27]  Gerhard Tröster,et al.  Pigeon Homing along Highways and Exits , 2004, Current Biology.

[28]  Jackie Chappell,et al.  Boldness traits, not dominance, predict exploratory flight range and homing behaviour in homing pigeons , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[29]  H. Maturana,et al.  Frontal and lateral visual system in birds. Frontal and lateral gaze. , 1988, Brain, behavior and evolution.

[30]  J. Henderson Human gaze control during real-world scene perception , 2003, Trends in Cognitive Sciences.

[31]  P. Green,et al.  HEAD-BOBBING DURING WALKING, RUNNING AND FLYING: RELATIVE MOTION PERCEPTION IN THE PIGEON , 1988 .

[32]  Alexei L. Vyssotski,et al.  Evidence that birds sleep in mid-flight , 2016, Nature Communications.

[33]  B. Frost,et al.  Head-bobbing in pigeons: how stable is the hold phase? , 2000, The Journal of experimental biology.

[34]  M. Land Motion and vision: why animals move their eyes , 1999, Journal of Comparative Physiology A.

[35]  Marian Stamp Dawkins,et al.  Pattern recognition and active vision in chickens , 2000, Nature.

[36]  Turgut Meydan,et al.  Enhanced Tracking System Based on Micro Inertial Measurements Unit to Measure Sensorimotor Responses in Pigeons , 2016, IEEE Sensors Journal.

[37]  Alan M. Wilson,et al.  Flying in a flock comes at a cost in pigeons , 2011, Nature.

[38]  S. Kane,et al.  When hawks attack: animal-borne video studies of goshawk pursuit and prey-evasion strategies , 2015, Journal of Experimental Biology.

[39]  M. Tomasello,et al.  Great apes anticipate that other individuals will act according to false beliefs , 2016, Science.

[40]  Scott P. Johnson,et al.  Eye Tracking in Infancy Research , 2009, Developmental neuropsychology.

[41]  Andrew A. Biewener,et al.  Pigeons (C. livia) Follow Their Head during Turning Flight: Head Stabilization Underlies the Visual Control of Flight , 2017, Front. Neurosci..

[42]  D. Biro,et al.  Homing pigeons develop local route stereotypy , 2005, Proceedings of the Royal Society B: Biological Sciences.

[43]  J. Dickman,et al.  Vestibular gaze stabilization: different behavioral strategies for arboreal and terrestrial avians. , 2005, Journal of neurophysiology.

[44]  Martin Egelhaaf,et al.  Gaze Strategy in the Free Flying Zebra Finch (Taeniopygia guttata) , 2008, PloS one.

[45]  D R Warrick,et al.  Bird Maneuvering Flight: Blurred Bodies, Clear Heads1 , 2002, Integrative and comparative biology.

[46]  M. Walker,et al.  Evidence that pigeons orient to geomagnetic intensity during homing , 2007, Proceedings of the Royal Society B: Biological Sciences.

[47]  J. Krebs,et al.  Vigilance in the third dimension: head movement not scan duration varies in response to different predator models , 2007, Animal Behaviour.

[48]  D. Biro,et al.  Landscape complexity influences route-memory formation in navigating pigeons , 2014, Biology Letters.

[49]  Dora Biro,et al.  Familiar route loyalty implies visual pilotage in the homing pigeon. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Adrian L. R. Thomas,et al.  Terminal attack trajectories of peregrine falcons are described by the proportional navigation guidance law of missiles , 2017, Proceedings of the National Academy of Sciences.

[51]  R. Wiltschko,et al.  Point of decision: when do pigeons decide to head home? , 2009, Naturwissenschaften.

[52]  D. W. Pratt Saccadic eye movements are coordinated with head movements in walking chickens. , 1982, The Journal of experimental biology.

[53]  Stephen Roberts,et al.  Positional entropy during pigeon homing II: navigational interpretation of Bayesian latent state models. , 2004, Journal of theoretical biology.

[54]  Marian Stamp Dawkins,et al.  What are birds looking at? Head movements and eye use in chickens , 2002, Animal Behaviour.

[55]  P. Green,et al.  Head orientation in pigeons during landing flight , 1992, Vision Research.